Abstract
BackgroundViruses are the simplest replicating units, characterized by a limited number of coding genes and an exceptionally high rate of overlapping genes. We sought a unified evolutionary explanation that accounts for their genome sizes, gene overlapping and capsid properties.ResultsWe performed an unbiased statistical analysis of ~100 families within ~400 genera that comprise the currently known viral world. We found that the volume utilization of capsids is often low, and greatly varies among viral families. Furthermore, although viruses span three orders of magnitude in genome length, they almost never have over 1500 overlapping nucleotides, or over four significantly overlapping genes per virus.ConclusionsOur findings undermine the generality of the compression theory, which emphasizes optimal packing and length dependency to explain overlapping genes and capsid size in viral genomes. Instead, we propose that gene novelty and evolution exploration offer better explanations to size constraints and gene overlapping in all viruses.ReviewersThis article was reviewed by Arne Elofsson and David Kreil.Electronic supplementary materialThe online version of this article (doi:10.1186/s13062-016-0128-3) contains supplementary material, which is available to authorized users.
Highlights
Viruses are the simplest replicating units, characterized by a limited number of coding genes and an exceptionally high rate of overlapping genes
The landscape of overlapping genes and genome length the subject of gene overlapping has already been extensively studied (e.g., [34]), we present a revised assessment, based on the following considerations: (i) inclusion of all known viruses; (ii) unbiased sampling of the viral space based on well-curated taxa as reliable representatives of the viral world; (iii) dealing only with nontrivial overlapping events
We have shown that the negative correlation that exists between genome length and overlapping rate in viruses is merely a side effect of a broader phenomenon: the absolute amount of gene overlapping is strictly bounded across the entire viral spectrum (Fig. 2)
Summary
Viruses are the simplest replicating units, characterized by a limited number of coding genes and an exceptionally high rate of overlapping genes. We sought a unified evolutionary explanation that accounts for their genome sizes, gene overlapping and capsid properties. Some of the most significant properties of viruses are their small physical size and an exceptional amount of overlapping genes (OGs) relative to their genome length [1, 2]. The high mutation rate of RNA viruses is mostly due to the absence of a proof reading mechanism in their replicating enzymes (i.e., RNA polymerase) [6]. It has been shown that mutation rate is inversely correlated with genome length, in viruses [4, 7]. The fast evolution of viruses is dominated by many factors, including their high mutation rate [8], large population
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